Habitat properties are key drivers of Borrelia burgdorferi (s.l.) prevalence in Ixodes ricinus populations of deciduous forest fragments.

BACKGROUND: The tick Ixodes ricinus has considerable impact on the health of humans and other terrestrial animals because it transmits several tick-borne pathogens (TBPs) such as B. burgdorferi (sensu lato), which causes Lyme borreliosis (LB). Small forest patches of agricultural landscapes provide many ecosystem services and also the disservice of LB risk. Biotic interactions and environmental filtering shape tick host communities distinctively between specific regions of Europe, which makes evaluating the dilution effect hypothesis and its influence across various scales challenging. Latitude, macroclimate, landscape and habitat properties drive both hosts and ticks and are comparable metrics across Europe. Therefore, we instead assess these environmental drivers as indicators and determine their respective roles for the prevalence of B. burgdorferi in I. ricinus. METHODS: We sampled I. ricinus and measured environmental properties of macroclimate, landscape and habitat quality of forest patches in agricultural landscapes along a European macroclimatic gradient. We used linear mixed models to determine significant drivers and their relative importance for nymphal and adult B. burgdorferi prevalence. We suggest a new prevalence index, which is pool-size independent. RESULTS: During summer months, our prevalence index varied between 0 and 0.4 per forest patch, indicating a low to moderate disservice. Habitat properties exerted a fourfold larger influence on B. burgdorferi prevalence than macroclimate and landscape properties combined. Increasingly available ecotone habitat of focal forest patches diluted and edge density at landscape scale amplified B. burgdorferi prevalence. Indicators of habitat attractiveness for tick hosts (food resources and shelter) were the most important predictors within habitat patches. More diverse and abundant macro- and microhabitat had a diluting effect, as it presumably diversifies the niches for tick-hosts and decreases the probability of contact between ticks and their hosts and hence the transmission likelihood. CONCLUSIONS: Diluting effects of more diverse habitat patches would pose another reason to maintain or restore high biodiversity in forest patches of rural landscapes. We suggest classifying habitat patches by their regulating services as dilution and amplification habitat, which predominantly either decrease or increase B. burgdorferi prevalence at local and landscape scale and hence LB risk. Particular emphasis on promoting LB-diluting properties should be put on the management of those habitats that are frequently used by humans. In the light of these findings, climate change may be of little concern for LB risk at local scales, but this should be evaluated further.

Environmental drivers of Ixodes ricinus abundance in forest fragments of rural European landscapes.

BACKGROUND: The castor bean tick (Ixodes ricinus) transmits infectious diseases such as Lyme borreliosis, which constitutes an important ecosystem disservice. Despite many local studies, a comprehensive understanding of the key drivers of tick abundance at the continental scale is still lacking. We analyze a large set of environmental factors as potential drivers of I. ricinus abundance. Our multi-scale study was carried out in deciduous forest fragments dispersed within two contrasting rural landscapes of eight regions, along a macroclimatic gradient stretching from southern France to central Sweden and Estonia. We surveyed the abundance of I. ricinus, plant community composition, forest structure and soil properties and compiled data on landscape structure, macroclimate and habitat properties. We used linear mixed models to analyze patterns and derived the relative importance of the significant drivers. RESULTS: Many drivers had, on their own, either a moderate or small explanatory value for the abundance of I. ricinus, but combined they explained a substantial part of variation. This emphasizes the complex ecology of I. ricinus and the relevance of environmental factors for tick abundance. Macroclimate only explained a small fraction of variation, while properties of macro- and microhabitat, which buffer macroclimate, had a considerable impact on tick abundance. The amount of forest and the composition of the surrounding rural landscape were additionally important drivers of tick abundance. Functional (dispersules) and structural (density of tree and shrub layers) properties of the habitat patch played an important role. Various diversity metrics had only a small relative importance. Ontogenetic tick stages showed pronounced differences in their response. The abundance of nymphs and adults is explained by the preceding stage with a positive relationship, indicating a cumulative effect of drivers. CONCLUSIONS: Our findings suggest that the ecosystem disservices of tick-borne diseases, via the abundance of ticks, strongly depends on habitat properties and thus on how humans manage ecosystems from the scale of the microhabitat to the landscape. This study stresses the need to further evaluate the interaction between climate change and ecosystem management on I. ricinus abundance.

Evaluating Functional Diversity: Missing Trait Data and the Importance of Species Abundance Structure and Data Transformation.

Functional diversity (FD) is an important component of biodiversity that quantifies the difference in functional traits between organisms. However, FD studies are often limited by the availability of trait data and FD indices are sensitive to data gaps. The distribution of species abundance and trait data, and its transformation, may further affect the accuracy of indices when data is incomplete. Using an existing approach, we simulated the effects of missing trait data by gradually removing data from a plant, an ant and a bird community dataset (12, 59, and 8 plots containing 62, 297 and 238 species respectively). We ranked plots by FD values calculated from full datasets and then from our increasingly incomplete datasets and compared the ranking between the original and virtually reduced datasets to assess the accuracy of FD indices when used on datasets with increasingly missing data. Finally, we tested the accuracy of FD indices with and without data transformation, and the effect of missing trait data per plot or per the whole pool of species. FD indices became less accurate as the amount of missing data increased, with the loss of accuracy depending on the index. But, where transformation improved the normality of the trait data, FD values from incomplete datasets were more accurate than before transformation. The distribution of data and its transformation are therefore as important as data completeness and can even mitigate the effect of missing data. Since the effect of missing trait values pool-wise or plot-wise depends on the data distribution, the method should be decided case by case. Data distribution and data transformation should be given more careful consideration when designing, analysing and interpreting FD studies, especially where trait data are missing. To this end, we provide the R package "traitor" to facilitate assessments of missing trait data.

Long-term colonization ecology of forest-dwelling species in a fragmented rural landscape - dispersal versus establishment.

Species colonization in a new habitat patch is an efficiency indicator of biodiversity conservation. Colonization is a two-step process of dispersal and establishment, characterized by the compatibility of plant traits with landscape structure and habitat conditions. Therefore, ecological trait profiling of specialist species is initially required to estimate the relative importance of colonization filters. Old planted parks best satisfy the criteria of a newly created and structurally matured habitat for forest-dwelling plant species. We sampled species in 230 ancient deciduous forests (source habitat), 74 closed-canopy manor parks (target habitats), 151 linear wooded habitats (landscape corridors), and 97 open habitats (isolating matrix) in Estonia. We defined two species groups of interest: forest (107 species) and corridor specialists (53 species). An extra group of open habitat specialists was extracted for trait scaling. Differing from expectations, forest specialists have high plasticity in reproduction mechanisms: smaller seeds, larger dispersules, complementary selfing ability, and diversity of dispersal vectors. Forest specialists are shorter, less nutrient-demanding and mycorrhizal-dependent, stress-tolerant disturbance-sensitive competitors, while corridor specialists are large-seeded disturbance-tolerant competitors. About 40% of species from local species pools have immigrated into parks. The historic forest area, establishment-related traits, and stand quality enhance the colonization of forest specialists. The openness of landscape and mowing in the park facilitate corridor specialists. Species traits in parks vary between a forest and corridor specialist, except for earlier flowering and larger propagules. Forest species are not dispersal limited, but they continue to be limited by habitat properties even in the long term. Therefore, the shady parts of historic parks should be appreciated as important forest biodiversity-enhancing landscape structures. The habitat quality of secondary stands can be improved by nurturing a heterogeneous shrub and tree layer, and modest herb layer management.